Abstract

Sperm from Drosophila simulans that carry a sex-ratio distorter is preferentially lost from females' sperm-storage
organs. This suggests that sperm dumping is a major factor affecting sperm competition
in this species, and may have evolved in response to sex-ratio distorters.

Minireview

Meiotic drivers are genes that subvert the normal rules of inheritance to ensure that
they are present in more than their fair share of gametes in the next generation [1]. For example, the driver sex-ratio (SR) in the fruit fly Drosophila simulans is an X chromosome that is present in all the sperm produced by male carriers, thus
causing SR males to produce only daughters (Figure 1). This is because sperm carrying the Y chromosome in these males fails to develop
properly. Early genetic analyses suggested that these drivers should increase in frequency
in the population, as male carriers pass the driver on to all their offspring [1,2]. The SR was also predicted to outcompete normal X chromosomes because of the increased
number of offspring in the population receiving the driving X. Eventually, the driver
should reach such a high frequency that the population would consist entirely of females
– and would go extinct. In reality, drivers do not seem to spread to fixation. In
wild populations, drivers are often found at a low but stable frequency, and in laboratory
populations SR and other drivers are usually outcompeted by non-driving chromosomes
[2]. Furthermore, experimental studies have shown that this failure to spread is probably
caused by reduced competitive ability of driving males' sperm [3].

In males carrying SR, for example, the failure of the sperm that carry the Y chromosome
could reduce the total amount of functioning sperm produced. This in turn might reduce
the amount of sperm that the male transfers to a female. If a female mates with more
than one male, the sperm will mix inside her and compete to fertilize her eggs, and
the male transferring the most sperm is generally expected to fertilize the majority
of eggs [4]. Male carriers of sex-distorter genes, whose sperm production is limited by the killing
of non-driving sperm, may be poor sperm competitors as a result [5].

Previous work has indeed found that carriers of meiotic drivers are generally poor
sperm competitors compared with non-carrying males [3], and this is assumed to be due to direct competition between sperm, with males that
transfer more sperm being more successful. A recent paper by Angelard and co-workers
[6], published in BMC Evolutionary Biology, now challenges this assumption, by showing that female response to sperm quantity
may be more important than direct competition between the sperm.

Angelard and her colleagues investigated SR drive in D. simulans. They mated virgin females to either a male carrying the SR driver or a normal male.
They then removed and counted the sperm both in the uterus, indicating the amount
transferred, and in the female's sperm-storage site, indicating the amount stored
by the female for use in fertilizing eggs. Males that carried the SR driver were found
to transfer half the number of sperm of normal males. After 24 hours, the proportion
of a male's sperm in storage was the same, irrespective of male genotype. However,
four days after mating, there was a significantly greater drop in the number of stored
sperm from males carrying the SR driver (compared with that from normal males), suggesting
that the 'driving' sperm was preferentially discarded by females. The authors confirmed
that this effect was not simply due to a higher death rate of SR sperm in storage
by assaying sperm mortality rate. Although SR sperm did show a higher mortality rate
than normal sperm, the difference was not large enough to account for the observed
decrease in sperm numbers.

The authors could not determine directly whether the removal of SR males' sperm was
due to a specific response by females to sperm carrying the SR driver, or was simply
a response to receiving small ejaculates. There is little previous evidence that females
can detect meiotic drivers in sperm, and it therefore seems likely that D. simulans females were responding to the significantly smaller ejaculates transferred by SR
males. This possibility could be tested in future studies by using multiply mated
normal males, which transfer smaller ejaculates.

Angelard and co-workers also allowed females to remate with a second male, allowing
either sperm transfer or interrupting the mating to allow seminal fluid but not sperm
to be passed to the female. Seminal fluid contains a wide range of proteins that directly
affect sperm competition and sperm survival [7]. Previous work, mostly on the closely related D. melanogaster, suggests that both sperm and accessory fluid have strong impacts on the sperm stored
from the first mating [7]. In Angelard's study, however, the second mating did not affect the release of sperm
from the first mating, whereas the genotype of the first male had a very strong impact
[6].

It has been suggested that female responses to meiotic drivers may play an important
role in preventing their spread through populations. For example, females could remate
more often when there is a risk of mating with SR males, thereby promoting sperm competition
that reduces the paternity of SR males [8]. Although sperm dumping has previously been suggested as a major factor affecting
the outcome of sperm competition in D. melanogaster [9], this is the first time it has been proposed to directly regulate the spread of meiotic
driving genes. Indeed, this work raises the possibility that the preferential dumping
by females of sperm from small ejaculates might have evolved as a way to reduce the
risk of driving males fathering offspring. There are other possible explanations,
however. For example, sperm loss could be a by-product of selection for something
else; conditions in the female sperm-storage organ are potentially damaging to sperm,
and large ejaculates may be better able to buffer against female spermicide and hence
survive longer. Certainly the uterus of a female Drosophila is a very unfriendly environment for sperm, possibly as a side effect of mechanisms
for preventing infection taking hold in the vulnerable reproductive tract [10].

Angelard et al. [6] used strains of D. simulans that had been maintained in the laboratory for many generations, and throughout this
time adult females and males were kept together. As a result, females were unlikely
to ever run out of sperm. It would be interesting to examine whether differential
loss of sperm also occurs in wild populations harboring meiotic drivers. In some populations,
sperm may be a far more valuable resource for females, which might reduce their willingness
to dump it. In particular, in populations that harbor a high frequency of SR or other
sex-ratio distorters, males (and therefore sperm) may be in short supply. Under these
conditions, would females still dump sperm from small ejaculates? And if they did
not, would this increase the spread of the driver through the population? The work
by Angelard et al. brings evidence of an important new mechanism to work on meiotic drive, and should
stimulate further research in this area.